Amyloid precursor protein (APP) contributes to pathology in the SOD1G93A mouse model of amyotrophic lateral sclerosis

Human Molecular Genetics

Volumn 21, Issue 17, 2012, Pages 3871-3882

  Bryson, J Barney ^a,b   Hobbs, Carl ^b   Parsons, Michael J ^c   Bosch, Karen D ^b   Pandraud, Amelie ^a   Walsh, Frank S ^b   Doherty, Patrick ^b   Greensmith, Linda ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; COPPER ZINC SUPEROXIDE DISMUTASE; GLIAL FIBRILLARY ACIDIC PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CELL SURVIVAL; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GLIA CELL; GRIP STRENGTH; MALE; MOTONEURON; MOTOR PERFORMANCE; MOTOR UNIT; MOUSE; MUSCLE ATROPHY; MUSCLE CONTRACTILITY; MUSCLE DENERVATION; MUSCLE INNERVATION; NERVE CELL DEGENERATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SPINAL CORD;

AMINO ACID SUBSTITUTION; AMYLOID BETA-PROTEIN PRECURSOR; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; ATROPHY; BODY WEIGHT; CELL SURVIVAL; CROSSES, GENETIC; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LONGEVITY; MALE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MOTOR NEURONS; MUSCLE DENERVATION; MUSCLE FIBERS, SKELETAL; NEUROMUSCULAR JUNCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SOLUBILITY; SPINAL CORD; SUPEROXIDE DISMUTASE; UP-REGULATION;

EID: 84865063394     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds215     Document Type: Article

References (36)

1. Wijesekera, L.C. and Leigh, P.N. (2009) Amyotrophic lateral sclerosis. Orphanet J. Rare Dis., 4, 3.
2. Gurney, M.E., Pu, H., Chiu, A.Y., Dal Canto, M.C., Polchow, C.Y., Alexander, D.D., Caliendo, J., Hentati, A., Kwon, Y.W., Deng, H.X. et al. (1994) Motor neuron degeneration in mice that express a human Cu, Zn superoxide dismutase mutation. Science, 264, 1772-1775.
3. Vargas, M.R., Pehar, M., Cassina, P., Beckman, J.S. and Barbeito, L. (2006) Increased glutathione biosynthesis by Nrf2 activation in astrocytes prevents p75NTR-dependent motor neuron apoptosis. J. Neurochem., 97, 687-696.
4. Yamanaka, K., Boillee, S., Roberts, E.A., Garcia, M.L., McAlonis-Downes, M., Mikse, O.R., Cleveland, D.W. and Goldstein, L.S. (2008) Mutant SOD1 in cell types other than motor neurons and oligodendrocytes accelerates onset of disease in ALS mice. Proc. Natl Acad. Sci. USA, 105, 7594-7599.
5. Boillee, S., Vande Velde, C. and Cleveland, D.W. (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron, 52, 39-59.
6. Lobsiger, C.S., Boillee, S., McAlonis-Downes, M., Khan, A.M., Feltri, M.L., Yamanaka, K. and Cleveland, D.W. (2009) Schwann cells expressing dismutase active mutant SOD1 unexpectedly slow disease progression in ALS mice. Proc. Natl Acad. Sci. USA, 106, 4465-4470.
7. Dupuis, L. and Loeffler, J.P. (2009) Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models. Curr. Opin. Pharmacol., 9, 341-346.
8. Dobrowolny, G., Aucello, M., Rizzuto, E., Beccafico, S., Mammucari, C., Boncompagni, S., Belia, S., Wannenes, F., Nicoletti, C., Del Prete, Z. et al. (2008) Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab., 8, 425-436.
9. Wong, M. and Martin, L.J. (2010) Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum. Mol. Genet., 19, 2284-2302.
10. Dupuis, L., Gonzalez de Aguilar, J.L., di Scala, F., Rene, F., de Tapia, M., Pradat, P.F., Lacomblez, L., Seihlan, D., Prinjha, R., Walsh, F.S. et al. (2002) Nogo provides a molecular marker for diagnosis of amyotrophic lateral sclerosis. Neurobiol. Dis., 10, 358-365.
11. Jokic, N., Gonzalez de Aguilar, J.L., Dimou, L., Lin, S., Fergani, A., Ruegg, M.A., Schwab, M.E., Dupuis, L. and Loeffler, J.P. (2006) The neurite outgrowth inhibitor Nogo-A promotes denervation in an amyotrophic lateral sclerosis model. EMBO Rep., 7, 1162-1167.
12. Fischer, L.R., Culver, D.G., Tennant, P., Davis, A.A., Wang, M., Castellano-Sanchez, A., Khan, J., Polak, M.A. and Glass, J.D. (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol., 185, 232-240.
13. Frey, D., Schneider, C., Xu, L., Borg, J., Spooren, W. and Caroni, P. (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci., 20, 2534-2542.
14. Pun, S., Santos, A.F., Saxena, S., Xu, L. and Caroni, P. (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat. Neurosci., 9, 408-419.
15. Atkin, J.D., Scott, R.L., West, J.M., Lopes, E., Quah, A.K. and Cheema, S.S. (2005) Properties of slow- and fast-twitch muscle fibres in a mouse model of amyotrophic lateral sclerosis. Neuromuscul. Disord., 15, 377-388.
16. Hegedus, J., Putman, C.T., Tyreman, N. and Gordon, T. (2008) Preferential motor unit loss in the SOD1 G93A transgenic mouse model of amyotrophic lateral sclerosis. J. Physiol., 586, 3337-3351.
17. Schaefer, A.M., Sanes, J.R. and Lichtman, J.W. (2005) A compensatory subpopulation of motor neurons in a mouse model of amyotrophic lateral sclerosis. J. Comp. Neurol., 490, 209-219.
18. Koistinen, H., Prinjha, R., Soden, P., Harper, A., Banner, S.J., Pradat, P.F., Loeffler, J.P. and Dingwall, C. (2006) Elevated levels of amyloid precursor protein in muscle of patients with amyotrophic lateral sclerosis and a mouse model of the disease. Muscle Nerve, 34, 444-450.
19. McFerrin, J., Engel, W.K. and Askanas, V. (1998) Impaired innervation of cultured human muscle overexpressing betaAPP experimentally and genetically: relevance to inclusion-body myopathies. Neuroreport, 9, 3201-3205.
20. Sugarman, M.C., Yamasaki, T.R., Oddo, S., Echegoyen, J.C., Murphy, M.P., Golde, T.E., Jannatipour, M., Leissring, M.A. and LaFerla, F.M. (2002) Inclusion body myositis-like phenotype induced by transgenic overexpression of beta APP in skeletal muscle. Proc. Natl Acad. Sci. USA, 99, 6334-6339.
21. Wirths, O., Weis, J., Kayed, R., Saido, T.C. and Bayer, T.A. (2007) Age-dependent axonal degeneration in an Alzheimer mouse model. Neurobiol. Aging, 28, 1689-1699.
22. Seo, J.S., Leem, Y.H., Lee, K.W., Kim, S.W., Lee, J.K. and Han, P.L. (2010) Severe motor neuron degeneration in the spinal cord of the Tg2576 mouse model of Alzheimer disease. J. Alzheimers Dis., 21, 263-276.
23. Yoo, Y.E. and Ko, C.P. (2011) Treatment with trichostatin A initiated after disease onset delays disease progression and increases survival in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol., 231, 147-159.
24. Gregorevic, P., Meznarich, N.A., Blankinship, M.J., Crawford, R.W. and Chamberlain, J.S. (2008) Fluorophore-labeled myosin-specific antibodies simplify muscle-fiber phenotyping. Muscle Nerve, 37, 104-106.
25. Zheng, H., Jiang, M., Trumbauer, M.E., Sirinathsinghji, D.J., Hopkins, R., Smith, D.W., Heavens, R.P., Dawson, G.R., Boyce, S., Conner, M.W. et al. (1995) beta-Amyloid precursor protein-deficient mice show reactive gliosis and decreased locomotor activity. Cell, 81, 525-531.
26. Kieran, D., Kalmar, B., Dick, J.R., Riddoch-Contreras, J., Burnstock, G. and Greensmith, L. (2004) Treatment with arimoclomol, a coinducer of heat shock proteins, delays disease progression in ALS mice. Nat. Med., 10, 402-405.
27. Sharp, P.S., Dick, J.R. and Greensmith, L. (2005) The effect of peripheral nerve injury on disease progression in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neuroscience, 130, 897-910.
28. Buller, A.J., Eccles, J.C. and Eccles, R.M. (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J. Physiol., 150, 417-439.
29. Ausoni, S., Gorza, L., Schiaffino, S., Gundersen, K. and Lomo, T. (1990) Expression of myosin heavy chain isoforms in stimulated fast and slow rat muscles. J. Neurosci., 10, 153-160.
30. Calingasan, N.Y., Chen, J., Kiaei, M. and Beal, M.F. (2005) Beta-amyloid 42 accumulation in the lumbar spinal cord motor neurons of amyotrophic lateral sclerosis patients. Neurobiol. Dis., 19, 340-347.
31. Wang, P., Yang, G., Mosier, D.R., Chang, P., Zaidi, T., Gong, Y.D., Zhao, N.M., Dominguez, B., Lee, K.F., Gan, W.B. et al. (2005) Defective neuromuscular synapses in mice lacking amyloid precursor protein (APP) and APP-Like protein 2. J. Neurosci., 25, 1219-1225.
32. Nikolaev, A., McLaughlin, T., O'Leary, D.D. and Tessier-Lavigne, M. (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature, 457, 981-989.
33. Filbin, M.T. (2003) Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci., 4, 703-713.
34. Wojcik, S., Engel, W.K., Yan, R., McFerrin, J. and Askanas, V. (2007) NOGO is increased and binds to BACE1 in sporadic inclusion-body myositis and in A beta PP-overexpressing cultured human muscle fibers. Acta Neuropathol., 114, 517-526.
35. Yang, Y.S., Harel, N.Y. and Strittmatter, S.M. (2009) Reticulon-4A (Nogo-A) redistributes protein disulfide isomerase to protect mice from SOD1-dependent amyotrophic lateral sclerosis. J. Neurosci., 29, 13850-13859.
36. Muresan, V., Varvel, N.H., Lamb, B.T. and Muresan, Z. (2009) The cleavage products of amyloid-beta precursor protein are sorted to distinct carrier vesicles that are independently transported within neurites. J. Neurosci., 29, 3565-3578.